Genetic Variability of Flight Metabolism in DROSOPHILA MELANOGASTER . II. Relationship between Power Output and Enzyme Activity Levels

The major goal of the studies reported here was to determine the extent to which genetic variation in the activities of the enzymes participating in flight metabolism contributes to variation in the mechanical power output of the flight muscles in Drosophila melanogaster. Isogenic chromosome substitution lines were used to partition the variance of both types of quantitative trait into genetic and environmental components. The mechanical power output was estimated from the wingbeat frequency, wing amplitude and wing morphology of tethered flies by applying the aerodynamic models of Weis-Fogh and Ellington. There were three major results. (1) Chromosomes sampled from natural populations provide a large and repeatable genetic component to the variation in the activities of most of the 15 flight metabolism enzymes investigated and to the variation in the mechanical power output of the flight muscles. (2) The mechanical power output is a sensitive indicator of the rate of flight metabolism (i.e., rate of oxygen consumption during tethered flight). (3) In spite of (1) and (2), no convincing cases of individual enzyme effects on power output were detected, although the number and sign of the significant enzyme-power correlations suggests that such effects are not totally lacking.     

Development of flight behaviour in maturing adults of Locusta migratoria: I. Flight performance and wing-stroke parameters

In tethered Locusta migratoria suspended from a flight balance, flight performance, wing-stroke frequency, stroke angle, and stroke plane angle were studied throughout adult life. No correlation between flight performance and age was found in adults older than 2 days. During continuous flight in locusts of all ages the wing-stroke frequency and the wing-stroke angle of both wings decreases, and the wing-stroke plane angle (forewing) increases slightly. Within 2 weeks of adult life the wing-stroke frequency increases by a factor of ca. 2, whereas the wing-stroke angles and the stroke plane angles remain constant.     

Genetic Variability of Flight Metabolism in DROSOPHILA MELANOGASTER . III. Effects of Gpdh Allozymes and Environmental Temperature on Power Output

The effect of allozyme variation at the sn-glycerol-3-phosphate dehydrogenase (Gpdh) locus on variation in the mechanical power output of the flight muscles of Drosophila melanogaster was investigated. The influence of different rearing and flight temperatures and of their interactions with the Gpdh allozymic genotypes (allotypes) on flight ability also were analyzed. Populations from three continents were used, and Gpdh allotypes were generated from crosses between randomly paired isofemale lines made autozygous for each of the two alleles by inbreeding. Measurements made during tethered flight, together with wing morphology, were used to estimate power output using both Weis-Fogh's and Ellington's formulas. Analyses of variance (ANOVA) indicated significant main effects for both environmental components (rearing and flight temperatures) but for only one of the three genetic components (genetic backgrounds within continent); Gpdh allotypes and populations (continent of origin) were not significant. The interaction between rearing and flight temperature was highly significant, indicating some physiological adaptation. The effect of Gpdh allozymes depended on both rearing and flight temperature and was either significant or marginally so, depending on which set of formulas was used. In either case, the S/S allotype showed a 2-4% greater power output than the F/F allotype at low temperature for both interactions. In addition, the S/S allotype showed significantly greater power output than the F/F allotype among flies raised at 15 degrees and flown at 15 degrees, whereas the reverse was true for flies raised at 30 degrees and flown at 30 degrees. Significant differences among the three allotypes for GPDH activity level were found in general, with S/S having the highest, F/S intermediate and F/F the lowest activity, and an inverse relationship existed between rearing temperature and activity. The temperature effects on power output are consistent with the geographical and seasonal variation observed at the Gpdh locus in nature. In general, the results show that Gpdh can be considered a minor polygene affecting quantitative variation in the power output during flight and that genotype-by-environment interaction is an important component of that effect.     

Morphology, Velocity, and Intermittent Flight in Birds

Body size, pectoralis composition, aspect ratio of the wing,and forward speed affect the use of intermittent flight in birds.During intermittent non-flapping phases, birds extend theirwings and glide or flex their wings and bound. The pectoralismuscle is active during glides but not during bounds; activityin other primary flight muscles is variable. Mechanical power,altitude, and velocity vary among wingbeats in flapping phases;associated with this variation are changes in neuromuscularrecruitment, wingbeat frequency, amplitude, and gait. Speciesof intermediate body mass (35–158 g) tend to flap-glideat slower speeds and flap-bound at faster speeds, regardlessof the aspect ratio of their wings. Such behavior may reducemechanical power output relative to continuous flapping. Smallerspecies (<20 g) with wings of low aspect ratio may flap-boundat all speeds, yet existing models do not predict an aerodynamicadvantage for the flight style at slow speeds. The behaviorof these species appears to be due to wing shape rather thanpectoralis physiology. As body size increases among species,percent time spent flapping increases, and birds much largerthan 300 g do not flap-bound. This pattern may be explainedby adverse scaling of mass-specific power or lift per unit poweroutput available from flight muscles. The size limit for theability to bound intermittently may be offset somewhat by thescaling of pectoralis composition. The percentage of time spentflapping during intermittent flight also varies according toflight speed.     

Development of flight behaviour in maturing adults of Locusta migratoria: II. Aerodynamic parameters

In Locusta migratoria suspended from a flight balance, flight speed relative to the air and the lift were recorded throughout adult life. During continuous flight at all ages flight speed and lift decrease, but during maturation both aerodynamic parameters increase. These parameters appear to be dominated by the wing-stroke frequency in a more or less constant relationship. Locusts only 2 days old can maintain altitude in free flight. It is concluded that the basic neuronal flight pattern is determined at the last moult and that only the motoroutput frequency increases to approximately match the body weight, which increases with age.     

Flight performance of the moth, Manduca sexta, at variable gravity

The tethered and free flight of Manduca sexta were studied during period 1,2, and 0 times normal gravity (g) produced in an aeroplane by flying through parabolic trajectories. Moths in tethered flight did not change their aerodynamic output in response to increases or decreases in gravity. Some moths in free flight at 0 g maintained a position in the box by flying against a surface, or into the angle between two surfaces. In the absence of gravity as an orienting stimulus, the positive dorsophotic response to light was dominant. As the period of 0 g continued, moths were increasingly likely to periodically reduce the amplitude of their wingbeat and/or stop flying, for the equivalent of a few wingbeats. Only at 0 g, moths very occasionally spread their wings and floated freely for a few seconds. At 0 g moths retained control of rolling and yawing movements but stability in pitch was greatly reduced or absent.     

The Control of Mechanical Power in Insect Flight

SYNOPSIS. The cost of locomotion is rarely constant, but rathervaries as an animal changes speed and direction. Ultimately,the locomotory muscles of an animal must compensate for thesechanging requirements by varying the amount of mechanical powerthat they produce. In this paper, we consider the mechanismsby which the mechanical power generated by the asynchronousflight muscles of the fruit fly, Drosophila melanogaster, isregulated to match the changing requirements during flight controlbehaviors. Our data come from individual flies flown in a flightarena under conditions in which stroke kinematics, total metaboliccost, and flight force are simultaneously measured. In orderto increase force production, flies must increase wing beatfrequency and wing stroke amplitude. Theory predicts that thesekinematics changes should result in a roughly cubic increasein the mechanical power requirements for flight. However, themechanical energy generated by muscle should increase only linearlywith stroke amplitude and frequency. This discrepancy impliesthat flight muscles must either recruit myofibrils or increaseactivation in order to generate sufficient mechanical powerto sustain elevated force production. By comparing respirometricallymeasured total metabolic power with kinematically estimatedmechanical power, we have calculated that the stress in theflight muscles of Drosophila must increase by 50% to accommodatea doubling of flight force. Electrophysiological evidence suggeststhat this change in stress may be accomplished by an increasedneural drive to the asynchronous muscles, which in turn mayact to recruit additional cross bridges through an increasein cytosolic calcium.     

Flight motor pattern in flying and non-flying Phasmida

Summary The insect order Phasmida comprises species with a broad spectrum of wing morphism and flight ability. By monitoring the electrical activity of several pterothoracic muscles the motor output during tethered flight was recorded for several Phasmida, ranging from excellent fliers to non-winged species. Both winged and non-winged species can generate a motor pattern as judged by criteria used to identify the locust flight pattern. However, in non-fliers the probability of expressing this pattern, its duration and precision are reduced. The antagonistic activity of the chosen muscle pairs is clearly different from the motor output during leg movements, which argues for specific motoneuronal coordination released for different behavioural performances. The demonstration of flight motor output in all tested Phasmida indicates that neural structures including their functional connectivity can be maintained independently of the appropriate peripheral structures. With respect to evolution this supports the idea that central neuronal interactions can be more conservative compared to changes in the periphery. Abbreviations of species names and indication of sexes are given in the first paragraph of Results     

In Vivo Time-Resolved Microtomography Reveals the Mechanics of the Blowfly Flight Motor

Dipteran flies are amongst the smallest and most agile of flying animals. Their wings are driven indirectly by large power muscles, which cause cyclical deformations of the thorax that are amplified through the intricate wing hinge. Asymmetric flight manoeuvres are controlled by 13 pairs of steering muscles acting directly on the wing articulations. Collectively the steering muscles account for <3% of total flight muscle mass, raising the question of how they can modulate the vastly greater output of the power muscles during manoeuvres. Here we present the results of a synchrotron-based study performing micrometre-resolution, time-resolved microtomography on the 145 Hz wingbeat of blowflies. These data represent the first four-dimensional visualizations of an organism''s internal movements on sub-millisecond and micrometre scales. This technique allows us to visualize and measure the three-dimensional movements of five of the largest steering muscles, and to place these in the context of the deforming thoracic mechanism that the muscles actuate. Our visualizations show that the steering muscles operate through a diverse range of nonlinear mechanisms, revealing several unexpected features that could not have been identified using any other technique. The tendons of some steering muscles buckle on every wingbeat to accommodate high amplitude movements of the wing hinge. Other steering muscles absorb kinetic energy from an oscillating control linkage, which rotates at low wingbeat amplitude but translates at high wingbeat amplitude. Kinetic energy is distributed differently in these two modes of oscillation, which may play a role in asymmetric power management during flight control. Structural flexibility is known to be important to the aerodynamic efficiency of insect wings, and to the function of their indirect power muscles. We show that it is integral also to the operation of the steering muscles, and so to the functional flexibility of the insect flight motor.     

Hindlimb Motion during Steady Flight of the Lesser Dog-Faced Fruit Bat,Cynopterus brachyotis

In bats, the wing membrane is anchored not only to the body and forelimb, but also to the hindlimb. This attachment configuration gives bats the potential to modulate wing shape by moving the hindlimb, such as by joint movement at the hip or knee. Such movements could modulate lift, drag, or the pitching moment. In this study we address: 1) how the ankle translates through space during the wingbeat cycle; 2) whether amplitude of ankle motion is dependent upon flight speed; 3) how tension in the wing membrane pulls the ankle; and 4) whether wing membrane tension is responsible for driving ankle motion. We flew five individuals of the lesser dog-faced fruit bat, Cynopterus brachyotis (Family: Pteropodidae), in a wind tunnel and documented kinematics of the forelimb, hip, ankle, and trailing edge of the wing membrane. Based on kinematic analysis of hindlimb and forelimb movements, we found that: 1) during downstroke, the ankle moved ventrally and during upstroke the ankle moved dorsally; 2) there was considerable variation in amplitude of ankle motion, but amplitude did not correlate significantly with flight speed; 3) during downstroke, tension generated by the wing membrane acted to pull the ankle dorsally, and during upstroke, the wing membrane pulled laterally when taut and dorsally when relatively slack; and 4) wing membrane tension generally opposed dorsoventral ankle motion. We conclude that during forward flight in C. brachyotis, wing membrane tension does not power hindlimb motion; instead, we propose that hindlimb movements arise from muscle activity and/or inertial effects.     

二点委夜蛾飞行行为特征

【目的】本研究旨在阐明二点委夜蛾的飞行行为特征,丰富二点委夜蛾飞行生物学理论,提高其预测预报水平。【方法】利用昆虫飞行磨被动吊飞系统和主动飞行监测系统,系统研究了二点委夜蛾Athdtis lepigone(M(o|¨)schler)被动飞行能力和主动飞行意愿。【结果】成虫具有较强的被动飞行潜力。室内连续吊飞80 h,雌雄蛾最远飞行距离分别达106.71 km和148.32 km,最长飞行时间分别达43.05 h和40.01h,最快飞行速度分别达7.60 km/h和8.14 km/h。雄蛾飞行潜力显著强于雌蛾,体现在飞行距离和飞行时间显著高于雌蛾,但飞行速度差异不显著。成虫蛾龄显著影响成虫飞行能力。对不同蛾龄成虫吊飞12 h的结果表明,1日龄即具备一定的飞行能力,之后逐渐增强,3日龄时飞行能力最强,雌雄蛾平均飞行距离分别为29.61 km和27.55 km,飞行时间分别为10.04 h和9.46 h,平均飞行速度分别达2.76 kn/h和2.46km/h,4日龄成虫飞行能力开始下降,但不同性别间成虫飞行能力差异不显著。蛾龄间飞行能力差异主要是由于不同蛾龄成虫的强、弱飞行个体比例不同。二点委夜蛾主动飞行呈现明显的节律行为,飞行活动主要集中在暗期(19:00—次日5:00),在光期(5:00—19:00)基本不飞行。成虫初羽化(1日龄)主动飞行意愿增强,之后飞行活动减少,但产卵开始时主动飞行活动又开始增强,到7日龄达到峰值。【结论】二点委夜蛾成虫具有较强的飞行能力,其飞行能力受蛾龄,雌雄等因素影响;飞行具有明显的节律性。     

Aerodynamics and Energetics of Intermittent Flight in Birds

Hypotheses explaining the use of intermittent bounding and undulatingflight modes in birds are considered. Existing theoretical modelsof intermittent flight have assumed that the animal flies ata constant speed throughout. They predict that mean mechanicalpower in undulating (flap-gliding) flight is reduced comparedto steady flight over a broad range of speeds, but is reducedin bounding flight only at very high flight speeds. Lift generatedby the bird's body or tail has a small effect on power, butis insufficient to explain observations of bounding at intermediateflight speeds. Measurements on starlings Sturnus vulgaris inundulating flight in a wind tunnel show that flight speed variesby around ±1 m/sec during a flap-glide cycle. Dynamicenergy is used to quantify flight performance, and reveals thatthe geometry of the flight path depends upon wingbeat kinematics,and that neither flapping nor gliding phases are at constantspeed and angle to the horizontal. The bird gains both kineticand potential energy during the flapping phases. A new theoreticalmodel indicates that such speed variation can give significantsavings in mechanical power in both bounding and undulatingflight. Alternative hypotheses for intermittent flight includea gearing mechanism, based on duty factor, mediating musclepower or force output against aerodynamic requirements. Thiscould explain the use of bounding flight in hovering and climbingin small passerines. Both bounding and undulating confer otheradaptive benefits; undulating may be primitive in birds, butbounding may have evolved in response to flight performanceoptimization, or to factors such as unpredictability in responseto predation.     

Field Flight Dynamics of Hummingbirds during Territory Encroachment and Defense

Hummingbirds are known to defend food resources such as nectar sources from encroachment by competitors (including conspecifics). These competitive intraspecific interactions provide an opportunity to quantify the biomechanics of hummingbird flight performance during ecologically relevant natural behavior. We recorded the three-dimensional flight trajectories of Ruby-throated Hummingbirds defending, being chased from and freely departing from a feeder. These trajectories allowed us to compare natural flight performance to earlier laboratory measurements of maximum flight speed, aerodynamic force generation and power estimates. During field observation, hummingbirds rarely approached the maximal flight speeds previously reported from wind tunnel tests and never did so during level flight. However, the accelerations and rates of change in kinetic and potential energy we recorded indicate that these hummingbirds likely operated near the maximum of their flight force and metabolic power capabilities during these competitive interactions. Furthermore, although birds departing from the feeder while chased did so faster than freely-departing birds, these speed gains were accomplished by modulating kinetic and potential energy gains (or losses) rather than increasing overall power output, essentially trading altitude for speed during their evasive maneuver. Finally, the trajectories of defending birds were directed toward the position of the encroaching bird rather than the feeder.     

Flight characteristics of birds:

This is the first part of a study on flight characteristics of birds and presents an annotated list of flight speeds of 139 western Palearctic species. All measurements were taken with the same tracking radar and corrected for wind influence according to radar-tracked wind-measuring balloons. Graphical presentation of the birds' air speeds emphasizes the wide variation of speeds within species and allows easy comparison between taxonomic groups, species, and types of flight. Unlike theoretical predictions, speeds increase only slightly with size. The larger species seem to be increasingly limited to speeds close to their speed of minimum power consumption V_mp',. Released birds, apparently reluctant to depart with migratory speed, fly at considerably lower speeds than migrating conspecifics. While large birds seem to be limited to speeds around V _mp', smaller birds seem to be capable of selecting between various speeds, approaching predicted V _mp, when tending to remain airborne at low cost, but flying at much higher speeds when tending to make best progress at low cost (around predicted speed of maximum range V _mr,). Predictions of air speeds by aerodynamic models proved to be too low for small birds because the models do not account for the gain in speed attained by the reduction in profile drag during bounding flight of small passerines. The models predict excessive speeds for large birds because the power output available for flight seems to decline much more with size than previously assumed.     

Flight metabolism in carpenter bees and primary structure of their hypertrehalosaemic peptide

We measured the rate of oxygen consumption and carbon dioxide production as well as energy substrates in haemolymph and flight muscles of carpenter bees of the genus Xylocopa at rest and after tethered lift-generating flight. Flight of 2 min duration at an ambient temperature of 28○C elevated oxygen consumption about 70-fold above resting rate. The respiratory quotient during rest and flight was 1 indicating that carbohydrates were the exclusive substrate oxidised. This was corroborated by measurements of metabolism. Carbohydrates are in high concentrations in the haemolymph. This store was significantly diminished during a 10-min flight period. Whereas lipids did not contribute to energy provisions, the proline concentration in the haemolymph and in the flight muscles was significantly decreased upon flight, but the amount can only account for a very small contribution to overall flight metabolism. Polysaccharide reserves in flight muscles and whole abdomina are almost non-existent. However, earlier studies had identified the crop as a source of oligosaccharides (Louw and Nicolson 1983). Carbohydrate metabolism is influenced by a metabolic peptide from the corpus cardiacum. We could isolate a peptide from the corpora cardiaca of carpenter bees, which by retention time in HPLC and by its mass is very likely characterised as the octapeptide Scg-AKH-II (pGlu-Leu-Asn-Phe- Ser-Thr-Gly-Trp-NH₂) previously shown to occur in certain Orthoptera. This is the first member of the large AKH/RPCH family of peptides to be identified from a hymenopteran species. Injection of the synthetic peptide into adult carpenter bees caused carbohydrate mobilisation. We suggest that the peptide targets the high sugar stores in the crop and speculate that it may facilitate sugar passage rate through the digestive system.Electronic supplementary material Electronic supplementary material is available for this article at and accessible for authorised users.     

On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria

Many evolutionary ecological studies have documented sexual dimorphism in morphology or behaviour. However, to what extent a sex-specific morphology is used differently to realize a certain level of behavioural performance is only rarely tested. We experimentally quantified flight performance and wing kinematics (wing beat frequency and wing stroke amplitude) and flight morphology (thorax mass, body mass, forewing aspect ratio, and distance to centre of forewing area) in the butterfly Pararge aegeria (L.) using a tethered tarsal reflex induced flight set-up under laboratory conditions. On average, females showed higher flight performance than males, but frequency and amplitude did not differ. In both sexes, higher flight performance was partly determined by wing beat frequency but not by wing stroke amplitude. Dry body mass, thorax mass, and distance to centre of forewing area were negatively related to wing beat frequency. The relationship between aspect ratio and wing stroke amplitude was sex-specific: females with narrower wings produced higher amplitude whereas males show the opposite pattern. The results are discussed in relation to sexual differences in flight behaviour.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 675–687.     

Flight activity in the parasitoid waspNasonia vitripennis (Hymenoptera: Pteromalidae)

Flight activity in females of the parasitoid wasp Nasonia vitripennis(Walker) was examined by measuring still-air tethered flight. There was a large amount of variation among females in flight duration. The longest single flight (with no pauses of more than 5 s) was more than 2 h long. Mating status had a significant and large effect on flight: mated females flew twice as long as virgin females. There also was a slight but significant effect of age on flight, with 3-day-old females being less likely to fly than 1-day-old females. Flight duration was not affected by prior exposure to other females, to honey, or to a low or a high host density.     

Flight capability and fatty acid level in triacylglycerol of long-distance migratory adults of the common cutworm, Spodoptera litura

The larvae of Spodoptera litura were reared on an artificial diet, and the flight capability, and triacylglycerol (TG) level plus its fatty acid composition in 3-day-old sexually mature and non-fed adults were compared. In males, during 3 hr of tethered flight, the levels of abdominal TG and its fatty acid components did not change. But thereafter the TG and fatty acids, significantly unsaturated fatty acids in TG declined in their levels with the prolongation of flight, unsaturated fatty acids being exhausted preceding saturated fatty acid decline. When males were tested by tethered flight for 20 hr, some could fly for nearly the whole period, and were judged to be able to fly for approximately 24 hr, depending on the level of residual TG. Fatty aids in TG decreased in females similarly to males during tethered flight and some females with fully developed ovaries deposited eggs after 12 hr of flight similarly to non-flown individuals, which supports the long-distance flight capability even in sexually mature females. These results are discussed with regard to the overseas migration of this moth.     

Ambient temperature affects free-flight performance in the fruit fly Drosophila melanogaster

To gain insight into how temperature affects locomotor performance in insects, the limits of flight performance have been estimated in freely flying fruit flies Drosophila melanogaster by determining the maximum load that a fly could carry following take-off. At a low ambient temperature of 15 °C, muscle mechanical power output matches the minimum power requirements for hovering flight. Aerodynamic force production rises with increasing temperature and eventually saturates at a flight force that is roughly equal to 2.1 times the body mass. Within the two-fold range of different body sizes, maximum flight force production during free flight does not decrease with decreasing body size as suggested by standard aerodynamic theories. Estimations of flight muscle mechanical power output yields a peak performance of 110 W kg⁻¹ muscle tissue for short-burst flight that was measured at an ambient temperature of 30 °C. With respect to the uncertainties in estimating muscle mechanical power during free flight, the estimated values are similar to those that were published for flight under tethered flight conditions. Accepted: 5 January 1999